Human islet amyloid polypeptide fibril binding to catalase: A transmission electron microscopy and microplate study

TheScientificWorldJournal

Volumn 10, Issue , 2010, Pages 879-893

  Milton, Nathaniel G N ^a   Harris, J Robin ^b,c  

^a UNIVERSITY OF WESTMINSTER   (United Kingdom)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Amylin; Amyloid; Catalase; Diabetes; Fibril; Islet amyloid polypeptide; Noninsulin dependent diabetes mellitus (NIDDM; type II diabetes); Prion protein

Indexed keywords

ALANINE; AMYLIN; AMYLIN[1-37]; AMYLIN[20-29]; AMYLIN[24-29]; AMYLIN[8-37]; AMYLOID BETA PROTEIN; CATALASE; GLYCINE; ISOLEUCINE; PRION PROTEIN; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME BINDING; ENZYME INHIBITION; HUMAN; IMMUNOASSAY; MICROTITER PLATE ASSAY; MOLECULAR RECOGNITION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN BINDING; PROTEIN MOTIF; RAT; TRANSMISSION ELECTRON MICROSCOPY;

AMYLOID; ANIMALS; CATALASE; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; PROTEIN BINDING; RATS;

RATTUS;

EID: 77953452374     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2010.73     Document Type: Article

References (55)

1. Janson, J., Soeller, W.C., Roche, P.C., Nelson, R.T., Torchia, A.J., Kreutter, D.K., and Butler, P.C. (1996) Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide. Proc. Natl. Acad. Sci. U. S. A. 93, 7283-7288. (Pubitemid 26243541)
2. Höppener, J.W. and Lips, C.J. (2006) Role of islet amyloid in type 2 diabetes mellitus. Int. J. Biochem. Cell Biol. 38, 726-736. (Pubitemid 43363409)
3. Höppener, J.W., Ahrén, B., and Lips, C.J. (2000) Islet amyloid and type 2 diabetes mellitus. N. Engl. J. Med. 343, 411-419. (Pubitemid 30626125)
4. Glenner, G.G., Eanes, E.D., and Wiley, C.A. (1988) Amyloid fibrils formed from a segment of the pancreatic islet amyloid protein. Biochem. Biophys. Res. Commun. 155, 608-614.
5. Goldsbury, C., Goldie, K., Pellaud, J., Seelig, J., Frey, P., Müller, S.A., Kistler, J., Cooper, G.J., and Aebi, U. (2000) Amyloid fibril formation from full-length and fragments of amylin. J. Struct. Biol. 130, 352-362.
6. Konarkowska, B., Aitken, J.F., Kistler, J., Zhang, S., and Cooper, G.J. (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells. FEBS J. 273, 3614-3624. (Pubitemid 44086959)
7. Westermark, P., Wernstedt, C., Wilander, E., Hayden, D.W., O'Brien, T.D., and Johnson, K.H. (1987) Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. U. S. A. 84, 3881-3885. (Pubitemid 17088383)
8. Harris, J.R. (2005) The contribution of microscopy to the study of amyloid plaques and to amyloid-β fibrillogenesis. In: Alzheimer's Disease: Cellular and Molecular Aspects of Amyloid β. Subcellular Biochemistry. Vol. 38. Harris, R. and Fahrenholz, F., Eds. Springer Science. pp. 1-44.
9. Goldsbury, C.S., Cooper, G.J., Goldie, K.N., Müller, S.A., Saafi, E.L., Gruijters, W.T., Misur, M.P., Engel, A., Aebi, U., and Kistler, J. (1997) Polymorphic fibrillar assembly of human amylin. J. Struct. Biol. 119, 17-27. (Pubitemid 27294718)
10. Madine, J., Jack, E., Stockley, P.G., Radford, S.E., Serpell, L.C., and Middleton, D.A. (2008) Structural insights into the polymorphism of amyloid-like fibrils formed by region 20-29 of amylin revealed by solid-state NMR and X-ray fiber diffraction. J. Am. Chem. Soc. 130, 14990-15001.
11. Milton, N.G.N. and Harris, J.R. (2009) Polymorphism of amyloid-beta fibrils and its effects on human erythrocyte catalase binding. Micron 40, 800-810.
12. Prusiner, S.B. (1987) Prions causing degenerative neurological diseases. Annu. Rev. Med. 38, 381-398.
13. Stromer, T. and Serpell, L.C. (2005) Structure and morphology of the Alzheimer's amyloid fibril. Microsc. Res. Tech. 67, 210-217. (Pubitemid 41243637)
14. Kawahara, M., Kuroda, Y., Arispe, N., and Rojas, E. (2000) Alzheimer's beta-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line. J. Biol. Chem. 275, 14077-14083. (Pubitemid 30339682)
15. Lim, Y.A., Ittner, L.M., Lim, Y.L., and Götz, J. (2008) Human but not rat amylin shares neurotoxic properties with Abeta42 in long-term hippocampal and cortical cultures. FEBS Lett. 582, 2188-2194.
16. Bloch, K., Shichman, E., Vorobeychik, M., Bloch, D., and Vardi, P. (2007) Catalase expression in pancreatic alpha cells of diabetic and non-diabetic mice. Histochem. Cell Biol. 127, 227-232. (Pubitemid 46147277)
17. Konarkowska, B., Aitken, J.F., Kistler, J., Zhang, S., and Cooper, G.J. (2005) Thiol reducing compounds prevent human amylin-evoked cytotoxicity. FEBS J. 272, 4949-4959. (Pubitemid 41415118)
18. Fita, I. and Rossmann, M.G. (1985) The active center of catalase. J. Mol. Biol. 185, 21-37.
19. Kirkman, H.N. and Gaetani, G.F. (1984) Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH. Proc. Natl. Acad. Sci. U. S. A. 81, 4343-4347.
20. Harris, J.R. and Holzenburg, A. (1989) Transmission electron microscopic studies on the quaternary structure of human erythrocyte catalase. Micron Microsc. Acta 20, 223-238.
21. Harris, J.R., Engelhardt, H., Volker, S., and Holzenburg, A. (1993) Electron microscopy of human erythrocyte catalase: new two-dimensional crystal forms. J. Struct. Biol. 111, 22-33. (Pubitemid 23338203)
22. Harris, J.R. and Holzenburg, A. (1995) Human erythrocyte catalase: 2-D crystal nucleation and production of multiple crystal forms. J. Struct. Biol. 115, 102-112.
23. Safo, M.K., Musayev, F.N., Wu, S.H., Abraham, D.J., and Ko, T.P. (2001) Structure of tetragonal crystals of human erythrocyte catalase. Acta Crystallogr. D Biol. Crystallogr. 57, 1-7.
24. Milton, N.G.N. (1999) Amyloid-β binds catalase with high affinity and inhibits hydrogen peroxide breakdown. Biochem. J. 344, 293-296.
25. Milton, N.G.N., Mayor, N.P., and Rawlinson, J. (2001) Identification of amyloid-β binding sites using an antisense peptide approach. Neuroreport 12, 2561-2566. (Pubitemid 32682222)
26. Putnam, C.D., Arvai, A.S., Bourne, Y., and Tainer, J.A. (2000) Active and inhibited human catalase structures: ligand and NADPH binding and catalytic mechanism. J. Mol. Biol. 296, 295-309.
27. Góth, L., Lenkey, A., and Bigler, W.N. (2001) Blood catalase deficiency and diabetes in Hungary. Diabetes Care 24, 1839-1840.
28. Janciauskiene, S. and Ahrén, B. (2000) Fibrillar islet amyloid polypeptide differentially affects oxidative mechanisms and lipoprotein uptake in correlation with cytotoxicity in two insulin-producing cell lines. Biochem. Biophys. Res. Commun. 267, 619-625. (Pubitemid 30076848)
29. Lenzen, S. (2008) Oxidative stress: the vulnerable beta-cell. Biochem. Soc. Trans. 36, 343-347.
30. Takemoto, K., Tanaka, M., Iwata, H., Nishihara, R., Ishihara, K., Wang, D.H., Ogino, K., Taniuchi, K., and Masuoka, N. (2009) Low catalase activity in blood is associated with the diabetes caused by alloxan. Clin. Chim. Acta 407, 43-46.
31. Lupi, R., Del Guerra, S., Mancarella, R., Novelli, M., Valgimigli, L., Pedulli, G.F., Paolini, M., Soleti, A., Filipponi, F., Mosca, F., Boggi, U., Del Prato, S., Masiello, P., and Marchetti, P. (2007) Insulin secretion defects of human type 2 diabetic islets are corrected in vitro by a new reactive oxygen species scavenger. Diabetes Metab. 33, 340-345.
32. Roth, J.D., Maier, H., Chen, S., and Roland, B.L. (2009) Implications of amylin receptor agonism: integrated neurohormonal mechanisms and therapeutic applications. Arch. Neurol. 66, 306-310.
33. Harris, J.R. (2002) In vitro fibrillogenesis of the amyloid-β1-42 peptide: cholesterol potentiation and aspirin inhibition. Micron 33, 609-626.
34. Harris, J.R. (2007) Amyloid-β fibril formation in vitro. In Cell Biology Protocols. Harris, J.R., Graham, J., and Rickwood, D., Eds. John Wiley & Sons, Chichester, U.K. pp. 345-347.
35. Harris, J.R. (1997) Negative Staining and Cryoelectron Microscopy: the Thin Film Techniques. Royal Microscopical Society Handbook No. 35. Bios Scientific Publishers, Oxford.
36. Milton, N.G.N. (2001) Inhibition of catalase activity with 3-amino-triazole enhances the cytotoxicity of the Alzheimer's amyloid-β peptide. Neurotoxicology 22, 767-774.
37. Kudva, Y.C., Mueske, C., Butler, P.C., and Eberhardt, N.L. (1998) A novel assay in vitro of human islet amyloid polypeptide amyloidogenesis and effects of insulin secretory vesicle peptides on amyloid formation. Biochem J. 331, 809-813.
38. Friguet, B., Chaffotte, A.F., Djavadi-Ohaniance, L., and Goldberg, M.E. (1985) Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay. J. Immunol. Methods 77, 305-319. (Pubitemid 15103678)
39. Luca, S., Yau, W.M., Leapman, R., and Tycko, R. (2007) Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry 46, 13505-13522. (Pubitemid 350209947)
40. Nanga, R.P., Brender, J.R., Xu, J., Hartman, K., Subramanian, V., and Ramamoorthy, A. (2009) Three-dimensional structure and orientation of rat islet amyloid polypeptide protein in a membrane environment by solution NMR spectroscopy. J. Am. Chem. Soc. 131, 8252-8261.
41. Westermark, P., Engström, U., Johnson, K.H., Westermark, G.T., and Betsholtz, C. (1990) Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc. Natl. Acad. Sci. U. S. A. 87, 5036-5040. (Pubitemid 20224267)
42. Higham, C.E., Jaikaran, E.T., Fraser, P.E., Gross, M., and Clark, A. (2000) Preparation of synthetic human islet amyloid polypeptide (IAPP) in a stable conformation to enable study of conversion to amyloid-like fibrils. FEBS Lett. 470, 55-60. (Pubitemid 30155623)
43. Kajava, A.V., Aebi, U., and Steven, A.C. (2005) The parallel superpleated beta-structure as a model for amyloid fibrils of human amylin. J. Mol. Biol. 348, 247-252. (Pubitemid 40462093)
44. Mothes, E., Shoeman, R.L., Schröder, R.R., and Traub, P. (1990) Polymerizing properties of pepstatin A. J. Struct. Biol. 105, 80-91.
45. Chander, H., Chauhan, A., Wegiel, J., Malik, M., Sheikh, A., and Chauhan, V. (2006) Binding of trypsin to fibrillar amyloid beta-protein. Brain Res. 1082, 173-181.
46. Clementi, M.E., Martorana, G.E., Pezzotti, M., Giardina, B., and Misiti, F. (2004) Methionine 35 oxidation reduces toxic effects of the amyloid beta-protein fragment (31-35) on human red blood cell. Int. J. Biochem. Cell Biol. 36, 2066-2076. (Pubitemid 38760035)
47. Kaminsky, Y.G. and Kosenko, E.A. (2008) Effects of amyloid-beta peptides on hydrogen peroxide-metabolizing enzymes in rat brain in vivo. Free Radic. Res. 42, 564-573.
48. Milton, N.G.N. (2004) Role of hydrogen peroxide in the aetiology of Alzheimer's disease: implications for treatment. Drugs Aging 21, 81-100. (Pubitemid 38294378)
49. Degasperi, G.R., Denis, R.G., Morari, J., Solon, C., Geloneze, B., Stabe, C., Pareja, J.C., Vercesi, A.E., and Velloso, L.A. (2009) Reactive oxygen species production is increased in the peripheral blood monocytes of obese patients. Metabolism 58, 1087-1095.
50. Jean, L., Lee, C.F., Lee, C., Shaw, M., and Vaux, D.J. (2010) Competing discrete interfacial effects are critical for amyloidogenesis. FASEB J. 24, 309-317.
51. Kolterman, O.G., Gottlieb, A., Moyses, C., and Colburn, W. (1995) Reduction of postprandial hyperglycemia in subjects with IDDM by intravenous infusion of AC137, a human amylin analogue. Diabetes Care 18, 1179-1182.
52. Pullman, J., Darsow, T., and Frias, J.P. (2006) Pramlintide in the management of insulin-using patients with type 2 and type 1 diabetes. Vasc. Health Risk Manag. 2, 203-212. (Pubitemid 44275457)
53. Vincent, H.K., Innes, K.E., and Vincent, K.R. (2007) Oxidative stress and potential interventions to reduce oxidative stress in overweight and obesity. Diabetes Obes. Metab. 9, 813-839.
54. Cort, J.R., Liu, Z., Lee, G.M., Huggins, K.N., Janes, S., Prickett, K., and Andersen, N.H. (2009) Solution state structures of human pancreatic amylin and pramlintide. Protein Eng. Des. Sel. 22, 497-513.
55. Nonoyama, A., Laurence, J.S., Garriques, L., Qi, H., Le, T., and Middaugh, C.R. (2008) A biophysical characterization of the peptide drug pramlintide (AC137) using empirical phase diagrams. J. Pharm. Sci. 97, 2552-2567.